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The molecular basis for flexibility in the flexible filamentous plant viruses

Nature Structural & Molecular Biology volume 22, pages 642–644 (2015)Cite this article

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Abstract

Flexible filamentous plant viruses cause more than half the viral crop damage in the world but are also potentially useful for biotechnology. Structural studies began more than 75 years ago but have failed, owing to the virion's extreme flexibility. We have used cryo-EM to generate an atomic model for bamboo mosaic virus, which reveals flexible N- and C-terminal extensions that allow deformation while still maintaining structural integrity.

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Figure 1: The BaMV helical capsid structure.
Figure 2: BaMV cryo-EM reconstruction allows building and refinement of atomic models.
Figure 3: The refined model reveals atomic details.

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Electron Microscopy Data Bank

Protein Data Bank

Referenced accessions

NCBI Reference Sequence

Protein Data Bank

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Acknowledgements

This work was supported by funds from US National Institutes of Health (NIH) GM035269, S10-RR025067 and S10-OD018149 (to E.H.E.); NSC98-2321-B-005-005-MY3 (to Y.-H.H.); NSC99-2628-B-001-012-MY3 and Academia Sinica (to N.-S.L.); and Scholarships for Excellent Students to Study Abroad from National Chung-Hsing University (to C.-C.C.). We thank K. Dryden for assistance with the cryo-EM. The cryo-EM work was conducted at the Molecular Electron Microscopy Core facility at the University of Virginia, which is supported by the School of Medicine and was built with NIH grant G20-RR31199. C.-C.C. thanks R.H. Cheng, L. Xing, R. Diaz, Z.H. Zhou and G.G. Liou for their assistance.

Author information

Author notes

  1. Frank DiMaio and Chun-Chieh Chen: These authors contributed equally to this work.

  2. yhhsu@dragon.nchu.edu.tw

Authors and Affiliations

  1. Department of Biochemistry, University of Washington, Seattle, Washington, USA

    Frank DiMaio & Brandon Frenz

  2. Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan

    Chun-Chieh Chen & Na-Sheng Lin

  3. Molecular and Biological Agricultural Sciences Program, Taiwan International Graduate Program, Academia Sinica, Taipei, Taiwan

    Chun-Chieh Chen & Na-Sheng Lin

  4. Graduate Institute of Biotechnology, National Chung-Hsing University, Taichung, Taiwan

    Chun-Chieh Chen & Yau-Heiu Hsu

  5. Department of Biochemistry and Molecular Genetics, University of Virginia, Charlottesville, Virginia, USA

    Xiong Yu & Edward H Egelman

  6. Biotechnology Center, National Chung-Hsing University, Taichung, Taiwan

    Na-Sheng Lin

Authors
  1. Frank DiMaio
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Contributions

C.-C.C. prepared the viral samples and did preliminary EM studies; Y.-H.H. and N.-S.L. initiated the studies, designed the viral constructs and provided guidance in the viral preparation; X.Y. did the EM and filament selection; E.H.E. did the image analysis and three-dimensional reconstruction; F.D. and B.F. did the molecular modeling; F.D. and E.H.E. wrote the paper; and all authors edited the manuscript.

Corresponding authors

Correspondence to Yau-Heiu Hsu, Na-Sheng Lin or Edward H Egelman.

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Competing interests

The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Power spectrum from BaMV segments.

A power spectrum generated from the 97,767 segments used in the final reconstruction (wt and Nd35 combined). The yellow arrow indicates the layer line (at 1/35.2 Å-1) arising from the left-handed one-start helix, while the red arrow indicates the fourth order of this one-start helical layer line at 1/8.8 Å-1. The log of the intensities is shown to allow for the large dynamic range.

Supplementary Figure 2 Map-map and model-map agreement.

(a) The FSC between the wildtype and Nd35 maps shows an apparent resolution of ~5.6 Å. (b) Models were fit to the wildtype maps (“training”) and evaluated against the Nd35 map (“testing”). The models show good agreement to both, with an FSC=0.5 crossing of about 5.0 Å, and with minimal overfitting (compare training map agreement to testing).

Supplementary Figure 3 Alternate views of the assembly, showing each subunit colored separately to better illustrate the intricate subunit interactions.

(a, b) Axial views of the assembly, looking from the top (a) and bottom (b) along the helical axis (referring to top and bottom from Figure 2). (c) The same view as in Figure 2c.

Supplementary Figure 4 Structure building and refinement are well converged.

(a) The best-scoring C-terminal models sampled by our backbone extension method show good convergence, with only small backbone deviations. (b,c) After all-atom refinement in the context of the full capsid, the best-scoring 5 models show minimal diversity in the core, with most of the diversity coming in the surface loops on the outside of the capsid (b), and the C-terminus on the inside of the capsid (c).

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–4 (PDF 641 kb)

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DiMaio, F., Chen, CC., Yu, X. et al. The molecular basis for flexibility in the flexible filamentous plant viruses. Nat Struct Mol Biol 22, 642–644 (2015). https://doi.org/10.1038/nsmb.3054

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